Differential impact of landscape-scale strategies for crop cultivar deployment on disease dynamics, resistance durability and long-term evolutionary control

Evolutionary Applications

Volumn 11, Issue 5, 2018, Pages 705-717

  Papaïx, Julien ^a   Rimbaud, Loup ^b   Burdon, Jeremy J ^b   Zhan, Jiasui ^c   Thrall, Peter H ^b  

^a INRA   (France)

^b CSIRO   (Australia)

^c FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

Author keywords

cropping ratio; durability; epidemiological control; landscape; resistance deployment strategy; spatial aggregation; spatially explicit model; susceptible exposed infectious removed

Indexed keywords

EID: 85036563466     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12570     Document Type: Article

References (76)

1. Allan, B., Keesing, F., & Ostfeld, R. (2003). Effect of forest fragmentation on lyme disease risk. Conservation Biology, 17, 267–272. https://doi.org/10.1046/j.1523-1739.2003.01260.x
2. Azzimonti, G. (2012) Diversification de la résistance quantitative à la rouille brune du blé à partir de la caractérisation des composantes de la résistance. PhD thesis, AgroParisTech, Paris, France.
3. Azzimonti, G., Lannou, C., Sache, I., & Goyeau, H. (2013). Components of quantitative resistance to leaf rust in wheat cultivars: Diversity, variability and specificity. Plant Pathology, 62, 970–981. https://doi.org/10.1111/ppa.2013.62.issue-5
4. Bennett, A. J., Bending, G. D., Chandler, D., Hilton, S., & Mills, P. (2012). Meeting the demand for crop production: The challenge of yield decline in crops grown in short rotations. Biological Reviews, 87, 52–71. https://doi.org/10.1111/brv.2012.87.issue-1
5. van den Berg, F., Lannou, C., Gilligan, C. A., & van den Bosch, F. (2013). Quantitative resistance can lead to evolutionary changes in traits not targeted by the resistance QTLs. Evolutionary Applications, 7, 370–380.
6. van den Bosch, F., & Gilligan, C. (2003). Measures of durability of resistance. Phytopathology, 93, 616–625. https://doi.org/10.1094/PHYTO.2003.93.5.616
7. Bourget, R., Chaumont, L., Durel, C.-E., & Sapoukhina, N. (2015). Sustainable deployment of QTLs conferring quantitative resistance to crops: First lessons from a stochastic model. New Phytologist, 206, 1163–1171. https://doi.org/10.1111/nph.2015.206.issue-3
8. Bourget, R., Chaumont, L., & Sapoukhina, N. (2013). Timing of pathogen adaptation to a multicomponent treatment. PLoS ONE, 8, e71926. https://doi.org/10.1371/journal.pone.0071926
9. Bouvier, A., Kiêu, K., Adamczyk, K., & Monod, H. (2009). Computation of the integrated flow of particles between polygons. Environmental Modelling & Software, 24, 843–849. https://doi.org/10.1016/j.envsoft.2008.11.006
10. Brown, J. K. M. (2015). Durable resistance of crops to disease: A Darwinian perspective. Annual Review of Phytopathology, 7, 609–624.
11. Brun, H., Chèvre, A.-M., Fitt, B. D., Powers, S., Besnard, A.-L., Ermel, M., … Andrivon, D. (2010). Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytologist, 185, 285–299. https://doi.org/10.1111/j.1469-8137.2009.03049.x
12. Burdon, J. J., Barrett, L. G., Rebetzke, G., & Thrall, P. H. (2014). Guiding deployment of resistance in cereals using evolutionary principles. Evolutionary Applications, 7, 609–624. https://doi.org/10.1111/eva.2014.7.issue-6
13. Burdon, J. J., & Thrall, P. H. (1999). Spatial and temporal patterns in coevolving plant and pathogen associations. The American Naturalist, 153, S15–S33. https://doi.org/10.1086/303209
14. Burdon, J. J., & Thrall, P. H. (2009). Coevolution of plants and their pathogens in natural habitats. Science, 324, 755–756. https://doi.org/10.1126/science.1171663
15. Burdon, J. J., Zhan, J. S., Barrett, L. G., Papaïx, J., & Thrall, P. H. (2016). Addressing the challenges of pathogen evolution on the worlds arable crop. Phytopathology, 106, 1117–1127. https://doi.org/10.1094/PHYTO-01-16-0036-FI
16. Chen, W., Wellings, C., Chen, X., Kang, Z., & Liu, T. (2014). Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici. Molecular Plant Pathology, 15, 433–446. https://doi.org/10.1111/mpp.2014.15.issue-5
17. Condeso, T. E., & Meentemeyer, R. K. (2007). Effects of landscape heterogeneity on the emerging forest disease sudden oak death. Journal of Ecology, 95, 364–375. https://doi.org/10.1111/jec.2007.95.issue-2
18. Débarre, F., & Gandon, S. (2010). Evolution of specialization in a spatially continuous environment. Journal of Evolutionary Biology, 23, 1090–1099. https://doi.org/10.1111/jeb.2010.23.issue-5
19. Débarre, F., & Gandon, S. (2011). Evolution in heterogeneous environments, between soft and hard selection. The American Naturalist, 177, E83–E97.
20. Fabre, F., Rousseau, E., Mailleret, L., & Moury, B. (2012). Durable strategies to deploy plant resistance in agricultural landscapes. New Phytologist, 193, 1064–1075. https://doi.org/10.1111/j.1469-8137.2011.04019.x
21. Fabre, F., Rousseau, E., Mailleret, L., & Moury, B. (2015). Epidemiological and evolutionary management of plant resistance: Optimizing the deployment of cultivar mixtures in time and space in agricultural landscapes. Evolutionary Applications, 8, 919–932. https://doi.org/10.1111/eva.2015.8.issue-10
22. Flor, H. H. (1955). Host-parasite interaction in flax rust. Its genetics and other implications. Phytopathology, 45, 680–685.
23. Gandon, S., Mackinnon, M. J., Nee, S., & Read, A. F. (2001). Imperfect vaccines and the evolution of pathogen virulence. Nature, 414, 751–756. https://doi.org/10.1038/414751a
24. Gilligan, C. A., & van den Bosch, F. (2008). Epidemiological models for invasion and persistence of pathogens. Annual Review of Phytopathology, 46, 385–418. https://doi.org/10.1146/annurev.phyto.45.062806.094357
25. Goyeau, H., & Lannou, C. (2011). Specific resistance to leaf rust expressed at the seedling stage in cultivars grown in France from 1983 to 2007. Euphytica, 178, 45–62. https://doi.org/10.1007/s10681-010-0261-5
26. Haas, S. E., Hooten, M. B., Rizzo, D. M., & Meentemeyer, R. K. (2011). Forest species diversity reduces disease risk in a generalist plant pathogen invasion. Ecology Letters, 14, 1108–1116. https://doi.org/10.1111/j.1461-0248.2011.01679.x
27. Holt, J., & Chancellor, T. C. B. (1999). Modelling the spatio-temporal deployment of resistant varieties to reduce the incidence of rice tungro disease in a dynamic cropping system. Plant Pathology, 48, 453–461. https://doi.org/10.1046/j.1365-3059.1999.00360.x
28. Johnson, R. (1983). Genetic background of durable resistance, Durable Resistance in Crops. Boston, MA: Springer New York.
29. Johnson, R. (1984). A critical analysis of durable resistance. Annual Review of Phytopathology, 22, 309–330. https://doi.org/10.1146/annurev.py.22.090184.001521
30. Jousimo, J., Tack, A. J. M., Ovaskainen, O., Mononen, T., Susi, H., Tollenaere, C., & Laine, A.-L. (2014). Ecological and evolutionary effects of fragmentation on infectious disease dynamics. Science, 344, 1289–1293. https://doi.org/10.1126/science.1253621
31. Kiêu, K., Adamczyk-Chauvat, K., Monod, H., & Stoica, R. S. (2013). A completely random T-tessellation model and Gibbsian extensions. Spatial Statistics, 6, 118–138. https://doi.org/10.1016/j.spasta.2013.09.003
32. Laine, A. L., & Barrès, B. (2013). Epidemiological and evolutionary consequences of life-history trade-offs in pathogens. Plant Pathology, 62(Suppl. 1), 96–105. https://doi.org/10.1111/ppa.2013.62.issue-S1
33. Laine, A.-L., Burdon, J. J., Dodds, P. N., & Thrall, P. H. (2011). Spatial variation in disease resistance: From molecules to metapopulations. Journal of Ecology, 99, 96–112. https://doi.org/10.1111/jec.2010.99.issue-1
34. Langlois, J., Fahrig, L., Merriam, G., & Artsob, H. (2001). Landscape structure influences continental distribution of hantavirus in deer mice. Landscape Ecology, 16, 255–266. https://doi.org/10.1023/A:1011148316537
35. Lannou, C. (2012). Variation and selection of quantitative traits in plant pathogens. Annual Review of Phytopathology, 50, 319–338. https://doi.org/10.1146/annurev-phyto-081211-173031
36. Leach, J. E., Cruz, C. M. V., Bai, J. F., & Leung, H. (2001). Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annual Review of Phytopathology, 39, 187–224. https://doi.org/10.1146/annurev.phyto.39.1.187
37. Leroy, T., Le Cam, B., & Lemaire, C. (2014). When virulence originates from non-agricultural hosts: New insights into plant breeding. Infection, Genetics and Evolution, 27, 521–529. https://doi.org/10.1016/j.meegid.2013.12.022
38. Lo Iacono, G., van den Bosh, F., & Paveley, N. (2012). The evolution of plant pathogens in response to host resistance: Factors affecting the gain from deployment of qualitative and quantitative resistance. Journal of Theoretical Biology, 304, 152–163. https://doi.org/10.1016/j.jtbi.2012.03.033
39. Lof, M. E., de Vallavieille-Pope, C., & van der Werf, W. (2017). Achieving durable resistance against plant diseases: Scenario analyses with a national-scale spatially explicit model for a wind-dispersed plant pathogen. Phytopathology, 107, 580–589. https://doi.org/10.1094/phyto-05-16-0207-r
40. McDonald, G. K., & Peck, D. (2009). Effects of crop rotation, residue retention and sowing time on the incidence and survival of ascochyta blight and its effect on grain yield of field peas (Pisum sativum). Field Crops Research, 111, 11–21. https://doi.org/10.1016/j.fcr.2008.10.001
41. Meynard, J., Doré, T., & Lucas, P. (2002). Agronomic approach: Cropping systems and plant diseases. Comptes Rendus Biologies, 326, 37–46.
42. Montarry, J., Cartier, E., Jacquemond, M., Palloix, A., & Moury, B. (2012). Virus adaptation to quantitative plant resistance: Erosion or breakdown? Journal of Evolutionary Biology, 25, 2242–2252. https://doi.org/10.1111/j.1420-9101.2012.02600.x
43. Mundt, C. C. (2002). Use of multiline cultivars and cultivar mixtures for disease management. Annual Review of Phytopathology, 40, 381–410. https://doi.org/10.1146/annurev.phyto.40.011402.113723
44. Mundt, C. C. (2014). Durable resistance: A key to sustainable management of pathogens and pests. Infection Genetics and Evolution, 27, 446–455. https://doi.org/10.1016/j.meegid.2014.01.011
45. Mundt, C. C., Leonard, K. J., Thal, W. M., & Fulton, J. H. (1986). Computerized simulation of crown rust epidemics in mixtures of immune and susceptible oat plants with different genotype unit area and spatial distributions of initial disease. Phytopathology, 76, 590–598. https://doi.org/10.1094/Phyto-76-590
46. Niks, R. E., Qi, X., & Marcel, T. C. (2015). Quantitative resistance to biotrophic filamentous plant pathogens: Concepts, misconceptions, and mechanisms. Annual Review of Phytopathology, 53, 445–470. https://doi.org/10.1146/annurev-phyto-080614-115928
47. Papaïx, J., Adamczyk-Chauvat, K., Bouvier, A., Kiêu, K., Touzeau, S., Lannou, C., & Monod, H. (2014). Pathogen population dynamics in agricultural landscapes: The Ddal modelling framework. Infection, Genetics and Evolution, 27, 509–520. https://doi.org/10.1016/j.meegid.2014.01.022
48. Papaïx, J., Burdon, J. J., Lannou, C., & Thrall, P. H. (2014). Evolution of pathogen specialisation in a host metapopulation: Joint effects of host and pathogen dispersal. PLoS Computational Biology, 10, e1003633. https://doi.org/10.1371/journal.pcbi.1003633
49. Papaïx, J., Burdon, J. J., Zhan, J. S., & Thrall, P. H. (2015). Crop pathogen emergence and evolution in agro-ecological landscapes. Evolutionary Applications, 8, 385–402. https://doi.org/10.1111/eva.12251
50. Papaïx, J., David, O., Lannou, C., & Monod, H. (2013). Dynamics of adaptation in spatially heterogeneous metapopulations. PLoS ONE, 8, e54697. https://doi.org/10.1371/journal.pone.0054697
51. Papaïx, J., Touzeau, S., Monod, H., & Lannou, C. (2014). Can epidemic control be achieved by altering landscape connectivity in agricultural systems? Ecological Modelling, 284, 35–47. https://doi.org/10.1016/j.ecolmodel.2014.04.014
52. Pariaud, B., Ravigné, V., Halkett, F., Goyeau, H., Carlier, J., & Lannou, C. (2009). Aggressiveness and its role in the adaptation of plant pathogens. Plant Pathology, 58, 409–424. https://doi.org/10.1111/ppa.2009.58.issue-3
53. Pariaud, B., Robert, C., Goyeau, H., & Lannou, C. (2009). Aggressiveness components and adaptation to a host cultivar in wheat leaf rust. Phytopathology, 99, 869–878. https://doi.org/10.1094/PHYTO-99-7-0869
54. Park, R. F. (2008). Breeding cereals for rust resistance in Australia. Plant Pathology, 57, 591–602. https://doi.org/10.1111/ppa.2008.57.issue-4
55. Parlevliet, J. E. (2002). Durability of resistance against fungal, bacterial and viral pathogens; present situation. Euphytica, 124, 147–156. https://doi.org/10.1023/A:1015601731446
56. Pietrevalle, S., Lemarié, S., & van den Bosch, F. (2006). Durability of resistance and cost of virulence. European Journal of Plant Pathology, 114, 107–116. https://doi.org/10.1007/s10658-005-3479-7
57. Pink, D., & Puddephat, I. (1999). Deployment of disease resistance genes by plant transformation - a mix and match approach. Trends in Plant Science, 4, 71–75. https://doi.org/10.1016/S1360-1385(98)01372-7
58. Plantegenest, M., Le May, C., & Fabre, F. (2007). Landscape epidemiology of plant diseases. Journal of the Royal Society Interface, 4, 963–972. https://doi.org/10.1098/rsif.2007.1114
59. Polechová, J., Barton, N., & Marion, G. (2009). Species’ range: Adaptation in space and time. The American Naturalist, 174, E186–E204. https://doi.org/10.1086/605958
60. Ravigné, V., Dieckmann, U., & Olivieri, I. (2009). Live where you thrive: Joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity. The American Naturalist, 174, E141–E169. https://doi.org/10.1086/605369
61. Real, L. A., & Biek, R. (2007). Spatial dynamics and genetics of infectious diseases on heterogeneous landscapes. Journal of the Royal Society Interface, 4, 935–948. https://doi.org/10.1098/rsif.2007.1041
62. Rounsevell, M. D. A., & Arneth, A. (2011). Representing human behaviour and decisional processes in land system models as an integral component of the earth system. Global Environmental Change, 21, 840–843. https://doi.org/10.1016/j.gloenvcha.2011.04.010
63. Sapoukhina, N., Tyutyunov, Y., Sache, I., & Arditi, R. (2010). Spatially mixed crops to control the stratified dispersal of airborne fungal diseases. Ecological Modelling, 221, 2793–2800. https://doi.org/10.1016/j.ecolmodel.2010.08.020
64. Skelsey, P., Rossing, W. A. H., Kessel, G. J. T., & van der Werf, W. (2010). Invasion of Phytophthora infestans at the landscape level: How do spatial scale and weather modulate the consequences of spatial heterogeneity in host resistance? Phytopathology, 100, 1146–1161. https://doi.org/10.1094/PHYTO-06-09-0148
65. Smith, D. L., Ericson, L., & Burdon, J. J. (2003). Epidemiological patterns at multiple spatial scales: An 11-year study of a Triphragmium Ulmariae - Filipendula Ulmaria metapopulation. Journal of Ecology, 91, 890–903. https://doi.org/10.1046/j.1365-2745.2003.00811.x
66. Soubeyrand, S., Laine, A.-L., Hanski, I., & Penttinen, A. (2009). Spatiotemporal structure of host-pathogen interactions in a metapopulation. The American Naturalist, 174, 308–320. https://doi.org/10.1086/603624
67. Soubeyrand, S., Sache, I., Lannou, C., & Chadoeuf, J. (2007). A frailty model to assess plant disease spread from individual count data. Journal of Data Science, 5, 67–83.
68. Stuthman, D. D., Leonard, K. J., & Miller-Garvin, J. (2007). Breeding crops for durable resistance to disease. San Diego, United States: Academic Press. https://doi.org/10.1016/S0065-2113(07)95004-X
69. Sudret, B. (2008). Global sensitivity analysis using polynomials chaos expansions. Reliability Engineering & System Safety, 93, 964–979. https://doi.org/10.1016/j.ress.2007.04.002
70. Tack, J. M., & Laine, A.-L. (2014). Ecological and evolutionary implications of spatial heterogeneity during the off-season for a wild plant pathogen. New Phytologist, 202, 297–308. https://doi.org/10.1111/nph.12646
71. Thrall, P. H., & Burdon, J. J. (2003). Evolution of virulence in a plant host-pathogen metapopulation. Science, 299, 1735–1737. https://doi.org/10.1126/science.1080070
72. Thrall, P. H., Oakeshott, J. G., Fitt, G., Southerton, S., Burdon, J. J., Sheppard, A., … Denison, R. F. (2011). Evolution in agriculture: The application of evolutionary approaches to the management of biotic interactions in agro-ecosystems. Evolutionary Applications, 4, 200–215. https://doi.org/10.1111/j.1752-4571.2010.00179.x
73. Waggoner, P. E., & Berger, R. (1987). Defoliation, disease and growth. Phytopathology, 77, 393–398.
74. Zhan, J. S., Thrall, P. H., & Burdon, J. J. (2014). Achieving sustainable plant disease management through evolutionary principles. Trends in Plant Sciences, 19, 570–575. https://doi.org/10.1016/j.tplants.2014.04.010
75. Zhan, J. S., Thrall, P. H., Papaïx, J., Xie, L., & Burdon, J. J. (2015). Playing on a pathogens weakness: Using evolution to guide sustainable plant disease control strategies. Annual Review of Phytopathology, 53, 19–43. https://doi.org/10.1146/annurev-phyto-080614-120040
76. Zhu, Y., Chen, H., Fan, J., Wang, Y., Li, Y., Chen, J., … Mundt, C. C. (2000). Genetic diversity and disease control in rice. Nature, 406, 718–722. https://doi.org/10.1038/35021046